Unhealthy Phenotype as Indicated by Salivary Biomarkers: Glucose, Insulin, VEGF-A, and IL-12p70 in Obese Kuwaiti Adolescents

Affiliations

01 January 2016

-

doi: 10.1155/2016/6860240


Abstract

Objective: Here, we investigated the relationships between obesity and the salivary concentrations of insulin, glucose, and 20 metabolic biomarkers in Kuwaiti adolescents. Previously, we have shown that certain salivary metabolic markers can act as surrogates for blood concentrations.

Methods: Salivary samples of whole saliva were collected from 8,317 adolescents. Salivary glucose concentration was measured by a high-sensitivity glucose oxidase method implemented on a robotic chemical analyzer. The concentration of salivary insulin and 20 other metabolic biomarkers was assayed in 744 randomly selected saliva samples by multiplexed bead-based immunoassay.

Results: Obesity was seen in 26.5% of the adolescents. Salivary insulin predicting hyperinsulinemia occurred in 4.3% of normal-weight adolescents, 8.3% of overweight adolescents, and 25.7% of obese adolescents (p < 0.0001). Salivary glucose predicting hyperglycemia was found in only 3% of obese children and was not predictive (p = 0.89). Elevated salivary glucose and insulin occurring together was associated with elevated vascular endothelial growth factor and reduced salivary interleukin-12.

Conclusion: Considering the surrogate nature of salivary insulin and glucose, this study suggests that elevated insulin may be a dominant sign of metabolic disease in adolescent populations. It also appears that a proangiogenic environment may accompany elevated glucose in obese adolescents.


Figures


Similar articles

Salivary Biomarkers as Predictors of Obesity and Intermediate Hyperglycemia in Adolescents.

Alqaderi H, Hegazi F, Al-Mulla F, Chiu CJ, Kantarci A, Al-Ozairi E, Abu-Farha M, Bin-Hasan S, Alsumait A, Abubaker J, Devarajan S, Goodson JM, Hasturk H, Tavares M.Front Public Health. 2022 Jun 10;10:800373. doi: 10.3389/fpubh.2022.800373. eCollection 2022.PMID: 35757631 Free PMC article.

The salivary levels of leptin and interleukin-6 as potential inflammatory markers in children obesity.

Pîrsean C, Neguț C, Stefan-van Staden RI, Dinu-Pirvu CE, Armean P, Udeanu DI.PLoS One. 2019 Jan 3;14(1):e0210288. doi: 10.1371/journal.pone.0210288. eCollection 2019.PMID: 30605486 Free PMC article.

A Data Mining Approach Identified Salivary Biomarkers That Discriminate between Two Obesity Measures.

Shi P, Goodson JM.J Obes. 2019 May 19;2019:9570218. doi: 10.1155/2019/9570218. eCollection 2019.PMID: 31236292 Free PMC article.

Salivary Biomarkers in Pediatric Metabolic Disease Research.

Hartman ML, Goodson JM, Barake R, Alsmadi O, Al-Mutawa S, Ariga J, Soparkar P, Behbehani J, Behbehani K.Pediatr Endocrinol Rev. 2016 Mar;13(3):602-11.PMID: 27116847 Review.

Sleep efficiency as a determinant of insulin sensitivity in overweight and obese adolescents.

Dorenbos E, Rijks JM, Adam TC, Westerterp-Plantenga MS, Vreugdenhil AC.Diabetes Obes Metab. 2015 Sep;17 Suppl 1:90-8. doi: 10.1111/dom.12515.PMID: 26332973 Review.


Cited by

An official website of the United States government

Here's how you know 

NIH NLM Logo

Log in

 


 

  •  
  •  
  •  
  •  

Access keysNCBI HomepageMyNCBI HomepageMain ContentMain Navigation

pubmed logo

Search:0 results are available, use up and down arrow keys to navigate.Search

Advanced

User Guide

Search results

SaveEmail

Send to

  •  
  •  
  •  
  •  

Display options

 Abstract PubMed PMID 

full text links

full text provider logo

actions

Cite

Collections

 

share

  •  
  •  

 

page navigation

 Title & authors Abstract Figures Similar articles Cited by References Publication types MeSH terms Substances Related information LinkOut - more resources 

J Obes

  •  
  •  
  •  

. 2016;2016:6860240.

doi: 10.1155/2016/6860240. Epub 2016 Mar 16.

Unhealthy Phenotype as Indicated by Salivary Biomarkers: Glucose, Insulin, VEGF-A, and IL-12p70 in Obese Kuwaiti Adolescents

Mor-Li Hartman 1J Max Goodson 1Ping Shi 1Jorel Vargas 1Tina Yaskell 1Danielle Stephens 1Maryann Cugini 1Hatice Hasturk 1Roula Barake 2Osama Alsmadi 3Sabiha Al-Mutawa 4Jitendra Ariga 4Pramod Soparkar 1Jawad Behbehani 5Kazem Behbehani 6Francine Welty 7

Affiliations expand

Free PMC article

Abstract

Objective: Here, we investigated the relationships between obesity and the salivary concentrations of insulin, glucose, and 20 metabolic biomarkers in Kuwaiti adolescents. Previously, we have shown that certain salivary metabolic markers can act as surrogates for blood concentrations.

Methods: Salivary samples of whole saliva were collected from 8,317 adolescents. Salivary glucose concentration was measured by a high-sensitivity glucose oxidase method implemented on a robotic chemical analyzer. The concentration of salivary insulin and 20 other metabolic biomarkers was assayed in 744 randomly selected saliva samples by multiplexed bead-based immunoassay.

Results: Obesity was seen in 26.5% of the adolescents. Salivary insulin predicting hyperinsulinemia occurred in 4.3% of normal-weight adolescents, 8.3% of overweight adolescents, and 25.7% of obese adolescents (p < 0.0001). Salivary glucose predicting hyperglycemia was found in only 3% of obese children and was not predictive (p = 0.89). Elevated salivary glucose and insulin occurring together was associated with elevated vascular endothelial growth factor and reduced salivary interleukin-12.

Conclusion: Considering the surrogate nature of salivary insulin and glucose, this study suggests that elevated insulin may be a dominant sign of metabolic disease in adolescent populations. It also appears that a proangiogenic environment may accompany elevated glucose in obese adolescents.

Figures

Figure 1

Figure 1

Semilogarithmic distribution of salivary glucose…

Figure 2

Figure 2

Percentage of the subset of…

Similar articles

Salivary Biomarkers as Predictors of Obesity and Intermediate Hyperglycemia in Adolescents.

Alqaderi H, Hegazi F, Al-Mulla F, Chiu CJ, Kantarci A, Al-Ozairi E, Abu-Farha M, Bin-Hasan S, Alsumait A, Abubaker J, Devarajan S, Goodson JM, Hasturk H, Tavares M.Front Public Health. 2022 Jun 10;10:800373. doi: 10.3389/fpubh.2022.800373. eCollection 2022.PMID: 35757631 Free PMC article.

The salivary levels of leptin and interleukin-6 as potential inflammatory markers in children obesity.

Pîrsean C, Neguț C, Stefan-van Staden RI, Dinu-Pirvu CE, Armean P, Udeanu DI.PLoS One. 2019 Jan 3;14(1):e0210288. doi: 10.1371/journal.pone.0210288. eCollection 2019.PMID: 30605486 Free PMC article.

A Data Mining Approach Identified Salivary Biomarkers That Discriminate between Two Obesity Measures.

Shi P, Goodson JM.J Obes. 2019 May 19;2019:9570218. doi: 10.1155/2019/9570218. eCollection 2019.PMID: 31236292 Free PMC article.

Salivary Biomarkers in Pediatric Metabolic Disease Research.

Hartman ML, Goodson JM, Barake R, Alsmadi O, Al-Mutawa S, Ariga J, Soparkar P, Behbehani J, Behbehani K.Pediatr Endocrinol Rev. 2016 Mar;13(3):602-11.PMID: 27116847 Review.

Sleep efficiency as a determinant of insulin sensitivity in overweight and obese adolescents.

Dorenbos E, Rijks JM, Adam TC, Westerterp-Plantenga MS, Vreugdenhil AC.Diabetes Obes Metab. 2015 Sep;17 Suppl 1:90-8. doi: 10.1111/dom.12515.PMID: 26332973 Review.

See all similar articles

Cited by

Salivary phosphate as a biomarker for human diseases.

Razzaque MS.FASEB Bioadv. 2022 Jan 3;4(2):102-108. doi: 10.1096/fba.2021-00104. eCollection 2022 Feb.PMID: 35141474 Free PMC article.

Salivary Redox Biomarkers in Insulin Resistance: Preclinical Studies in an Animal Model.

Maciejczyk M, Pawlukianiec C, Żendzian-Piotrowska M, Ładny JR, Zalewska A.Oxid Med Cell Longev. 2021 Sep 9;2021:3734252. doi: 10.1155/2021/3734252. eCollection 2021.PMID: 34557264 Free PMC article.

Caveolin-1 Variant Is Associated With the Metabolic Syndrome in Kuwaiti Children.

Nizam R, Al-Ozairi E, Goodson JM, Melhem M, Davidsson L, Alkhandari H, Al Madhoun A, Shamsah S, Qaddoumi M, Alghanim G, Alhasawi N, Abu-Farha M, Abubaker J, Shi P, Hartman ML, Tavares M, Bitar M, Ali H, Arefanian H, Devarajan S, Al-Refaei F, Alsmadi O, Tuomilehto J, Al-Mulla F.Front Genet. 2018 Dec 21;9:689. doi: 10.3389/fgene.2018.00689. eCollection 2018.PMID: 30622557 Free PMC article.

Associations of Salivary BPIFA1 Protein in Chronic Periodontitis Patients with Type 2 Diabetes Mellitus.

Guo Y, Guo LN, Zhu JF, Tang CY, Feng YZ, Zhou HD.Int J Endocrinol. 2017;2017:1087017. doi: 10.1155/2017/1087017. Epub 2017 Oct 4.PMID: 29109737 Free PMC article.

Saliva diagnostics - Current views and directions.

Kaczor-Urbanowicz KE, Martin Carreras-Presas C, Aro K, Tu M, Garcia-Godoy F, Wong DT.Exp Biol Med (Maywood). 2017 Mar;242(5):459-472. doi: 10.1177/1535370216681550. Epub 2016 Dec 8.PMID: 27903834 Free PMC article. Review.


KMEL References


References

  1.  
    1. Popkin B. M. Does global obesity represent a global public health challenge? The American Journal of Clinical Nutrition. 2011;93(2):232–233. doi: 10.3945/ajcn.110.008458. - DOI - PMC - PubMed
  2.  
    1. Freedman D. S., Khan L. K., Serdula M. K., Dietz W. H., Srinivasan S. R., Berenson G. S. The relation of childhood BMI to adult adiposity: the Bogalusa Heart study. Pediatrics. 2005;115(1):22–27. doi: 10.1542/peds.2004-0220. - DOI - PubMed
  3.  
    1. Halfon N., Larson K., Slusser W. Associations between obesity and comorbid mental health, developmental, and physical health conditions in a nationally representative sample of us children aged 10 to 17. Academic Pediatrics. 2013;13(1):6–13. doi: 10.1016/j.acap.2012.10.007. - DOI - PubMed
  4.  
    1. Reilly J. J., Kelly J. Long-term impact of overweight and obesity in childhood and adolescence on morbidity and premature mortality in adulthood: systematic review. International Journal of Obesity. 2011;35(7):891–898. doi: 10.1038/ijo.2010.222. - DOI - PubMed
  5.  
    1. Goodson J. M., Welty F. K. Using salivary biomarkers to identify children at risk of Type 2 diabetes. Diabetes Management. 2014;4(6):463–465. doi: 10.2217/dmt.14.34. - DOI
  6.  
    1. Foster G. D., Linder B., Baranowski T., et al. A school-based intervention for diabetes risk reduction. The New England Journal of Medicine. 2010;363(5):443–453. doi: 10.1056/nejmoa1001933. - DOI - PMC - PubMed
  7.  
    1. Goodson J. M., Kantarci A., Hartman M.-L., et al. Metabolic disease risk in children by salivary biomarker analysis. PLoS ONE. 2014;9(6) doi: 10.1371/journal.pone.0098799.e98799 - DOI - PMC - PubMed
  8.  
    1. Karageorgi S., Alsmadi O., Behbehani K. A review of adult obesity prevalence, trends, risk factors, and epidemiologic methods in Kuwait. Journal of Obesity. 2013;2013:14. doi: 10.1155/2013/378650.378650 - DOI - PMC - PubMed
  9.  
    1. International Diabetes Federation. IDF Diabetes Atlas. 5th. Brussels, Belgium: International Diabetes Federation; 2011.
  10.  
    1. Hartman M.-L., Goodson J. M., Barake R., et al. Salivary glucose concentration exhibits threshold kinetics in normal-weight, overweight, and obese children. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy. 2015;8:9–15. doi: 10.2147/dmso.s72744. - DOI - PMC - PubMed
  11.  
    1. Banerjee R. K., Datta A. G. Salivary peroxidases. Molecular and Cellular Biochemistry. 1986;70(1):21–29. - PubMed
  12.  
    1. Seidel A., Parker H., Turner R., et al. Uric acid and thiocyanate as competing substrates of lactoperoxidase. The Journal of Biological Chemistry. 2014;289(32):21937–21949. doi: 10.1074/jbc.m113.544957. - DOI - PMC - PubMed
  13.  
    1. Piombino P., Genovese A., Esposito S., et al. Saliva from obese individuals suppresses the release of aroma compounds from wine. PLoS ONE. 2014;9(1) doi: 10.1371/journal.pone.0085611.e85611 - DOI - PMC - PubMed
  14.  
    1. de Onis M., Onyango A. W., Borghi E., Siyam A., Nishida C., Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bulletin of the World Health Organization. 2007;85(9):660–667. doi: 10.2471/blt.07.043497. - DOI - PMC - PubMed
  15.  
    1. Zimmet P., Alberti G. K. M. M., Kaufman F., et al. The metabolic syndrome in children and adolescents—an IDF consensus report. Pediatric Diabetes. 2007;8(5):299–306. doi: 10.1111/j.1399-5448.2007.00271.x. - DOI - PubMed
  16.  
    1. Williams C. L., Hayman L. L., Daniels S. R., et al. Cardiovascular health in childhood: a statement for health professionals from the Committee on Atherosclerosis, Hypertension, and Obesity in the Young (AHOY) of the Council on Cardiovascular Disease in the Young, American Heart Association. Circulation. 2002;106(1):143–160. doi: 10.1161/01.cir.0000019555.61092.9e. - DOI - PubMed
  17.  
    1. Vukovic R., Milenkovic T., Mitrovic K., et al. Preserved insulin sensitivity predicts metabolically healthy obese phenotype in children and adolescents. European Journal of Pediatrics. 2015;174(12):1649–1655. doi: 10.1007/s00431-015-2587-4. - DOI - PubMed
  18.  
    1. Boucher J., Kleinridders A., Ronald Kahn C. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harbor Perspectives in Biology. 2014;6(1) doi: 10.1101/cshperspect.a009191.a009191 - DOI - PMC - PubMed
  19.  
    1. Blüher S., Schwarz P. Metabolically healthy obesity from childhood to adulthood—does weight status alone matter? Metabolism: Clinical and Experimental. 2014;63(9):1084–1092. doi: 10.1016/j.metabol.2014.06.009. - DOI - PubMed
  20.  
    1. Jessup A., Harrell J. S. The metabolic syndrome: look for it in children and adolescents, too! Clinical Diabetes. 2005;23(1):26–32. doi: 10.2337/diaclin.23.1.26. - DOI
  21.  
    1. Corkey B. E. Banting lecture 2011: hyperinsulinemia: cause or consequence? Diabetes. 2012;61(1):4–13. doi: 10.2337/db11-1483. - DOI - PMC - PubMed
  22.  
    1. Corkey B. E. Diabetes: have we got it all wrong? Insulin hypersecretion and food additives: cause of obesity and diabetes? Diabetes Care. 2012;35(12):2432–2437. doi: 10.2337/dc12-0825. - DOI - PMC - PubMed
  23.  
    1. Siervo M., Tomatis V., Stephan B. C. M., Feelisch M., Bluck L. J. C. VEGF is indirectly associated with NO production and acutely increases in response to hyperglycaemia. European Journal of Clinical Investigation. 2012;42(9):967–973. doi: 10.1111/j.1365-2362.2012.02684.x. - DOI - PubMed
  24.  
    1. Siervo M., Ruggiero D., Sorice R., et al. Body mass index is directly associated with biomarkers of angiogenesis and inflammation in children and adolescents. Nutrition. 2012;28(3):262–266. doi: 10.1016/j.nut.2011.06.007. - DOI - PubMed
  25.  
    1. Matsuda M., DeFronzo R. A. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–1470. doi: 10.2337/diacare.22.9.1462. - DOI - PubMed
  26.  
    1. Yuzhalin A. E., Kutikhin A. G. Interleukin-12: clinical usage and molecular markers of cancer susceptibility. Growth Factors. 2012;30(3):176–191. doi: 10.3109/08977194.2012.678843. - DOI - PubMed
  27.  
    1. Zorena K., Raczyńska D., Raczyńska K. Biomarkers in diabetic retinopathy and the therapeutic implications. Mediators of Inflammation. 2013;2013:11. doi: 10.1155/2013/193604.193604 - DOI - PMC - PubMed
  28.  
    1. Upile T., Jerjes W., Kafas P., et al. Salivary VEGF: a non-invasive angiogenic and lymphangiogenic proxy in head and neck cancer prognostication. International Archives of Medicine. 2009;2(1, article 12) doi: 10.1186/1755-7682-2-12. - DOI - PMC - PubMed
  29.  
    1. Byrne M. L., O'Brien-Simpson N. M., Reynolds E. C., et al. Acute phase protein and cytokine levels in serum and saliva: a comparison of detectable levels and correlations in a depressed and healthy adolescent sample. Brain, Behavior, and Immunity. 2013;34:164–175. doi: 10.1016/j.bbi.2013.08.010. - DOI - PubMed